Section 2 Snake Ecology

#### **Chapter 4**

## Ecology of Red-Tongue Viper (*Gloydius ussuriensis*) in Jeju Island, South Korea

*Hong-Shik Oh and Maniram Banjade*

#### **Abstract**

Understanding the ecology of species at risk is extremely important for their conservation and management. Due to land clearing for urban expansion, agriculture, and the import of pets, several snake species including the red-tongue viper (*Gloydius ussuriensis*) on Jeju Island of South Korea, have become threatened. We studied morphology, distribution, habitat characteristics, diet, and reproduction of red-tongue viper to provide a higher understanding of species ecology. This species on average reach 242–580 mm snout-vent length and is found in a wide range of habitat from mountain forest to lowland areas. Adult snakes prey almost entirely on amphibians followed by mammals and centipedes. The mating usually takes place in spring and birth takes place in autumn. This study points out the major threats and ill-information if addressed will not only contribute to the conservation efforts but also improve the negative attitudes that people hold toward these fascinating animals. The ecological data of *G. ussuriensis* herein provides basic information which assists in designing the management technique for conservation. Similar applications may be generalized and used to other vulnerable species to detect and quantify population ecology and risks, bolstering conservation methods that can be used to optimize the efficacy of conservation measures.

**Keywords:** *Gloydius ussuriensis*, viperidae, ecology, Jeju Island, threats

#### **1. Introduction**

Snakes have fascinated people for millennia. They have been integrated into a variety of myths and civilizations [1]. Despite having a limbless ectothermic body, snake species have spread throughout the Earth's biomes except for the polar area. Some species may still be found within the Arctic circle (e.g., *Vipera berus*; [2]). Snakes are one of the most misunderstood and mistreated animal species [3, 4]. Snake conservation has significant hurdles due to widespread unfavorable views of snakes and a lack of awareness of their basic biology [5]. Unfortunately, we frequently know the least about the species that are the most in need of protection because of their seeming scarcity. These difficulties are most evident for vipers (Family Viperidae, ~330 species). Vipers are species with a broad range of habitats. Only a few places such as Antarctica, Australia, New Zealand, Madagascar, the Arctic Circle, and island clusters like Hawaii are free of vipers.

Vipers are among the most poisonous family of snakes. They belong to the family Viperidae. All vipers are known for their long, hollow fangs that are hinged on a highly flexible maxillary bone. Vipers are also known for their phylogenetically extensive viviparity, parental care, and ambush forager behavior [6, 7]. In a study of 1500 randomly selected reptile species, Böhm et al. [8] have discovered that vipers are much more endangered than predicted. Even though vipers make up just 9% of all snakes [9], they account for 20% of 226 snakes classified as endangered on the International Union for Conservation of Nature (IUCN) Red List [10]. Twenty viper species are classified as vulnerable, 23 as endangered, and 11 as critically endangered globally [10].

#### **1.1 Snakes in South Korea**

Snakes in South Korea live like in any Asian country. The location of the country is in a temperate climatic zone that provides a territory with rich flora and fauna. The country's heterogeneous landscape is represented by plains, mountains, and sea coast. Rich forests are found not only in the plains, but also in the foothills and mountainous regions which provide excellent feeding, resting, and spawning habitats for a variety of animals as well as various herpetofauna, particularly snakes. South Korea is home to 20 species of both poisonous and non-poisonous snakes (**Table 1**). Of 600 species of venomous snakes worldwide, South Korea is home to nine species [11, 12]. These venomous snakes include three pit vipers (*Gloydius brevicaudus*, *G. ussuriensis*, and *Gloydius intermedius*) belonging to Viperidae, *Rhabdophis* 


### **Table 1.**

*List of snake species in South Korea.*

#### *Ecology of Red-Tongue Viper (*Gloydius ussuriensis*) in Jeju Island, South Korea DOI: http://dx.doi.org/10.5772/intechopen.101277*

*tigrinus* belonging to Colubridae, and five marine species belonging to Elapidae [13]. Red-tongue viper (*G. ussuriensis*) has the highest venom toxicity among pit vipers based on LD50 (lethal dose that kills 50% of the population) values, followed by *G. intermedius* and *G. brevicaudus* [14]. The venom of *G. ussuriensis*, like those of other viperids, is hemotoxic, causing hemorrhages, thromboses, and severe necrosis [14]. *G. ussuriensis* and *G. brevicaudus* are the two species responsible for the majority of snakebite incidents in South Korea, particularly the former. According to large data from Korea's Health Insurance Review & Assessment Service, poisonous snake bites impact 2315–4143 patients on average each year in South Korea.

In South Korea, *G. ussuriensis* (**Figure 1**) has a wide distribution, including the mainland of South Korea and its associated islands. Jeju, the largest Island that is rich in biodiversity, is located 73 km south of the Korean Peninsula. It is a wellknown habitat for this species. However, rapid urbanization and industrialization have posed a threat to this species. In the previous two decades, Jeju Island has seen significant urbanization and industrialization, undergoing a large-scale change from agricultural land to industrial land for civilization [15]. The use of heavy equipment for farming, land clearance, and road construction has caused their high mortality. Moreover, they are killed by humans despite their important roles as prey and predators in the ecosystem. These species account for a substantial proportion of middle-order predators that keep our natural ecosystem working.

However, a comprehensive understanding of its ecology and population biology is lacking. Such gaps in our understanding hinder our capacity to design effective conservation and management plans. They also prevent us from arguing that conservation is even necessary. This seems to be because there is a lack of communication between scientists due to publications written in various languages. Most publications about *G. ussuriensis* are in the Korean language, attracting little attention from researchers who write in western languages. In an attempt to bring Korean research focusing on *G. ussuriensis* to the attention of researchers worldwide, we reviewed various publications and major findings of Kim and Oh from 2014 to 2016. Effective conservation of snakes nearly always requires answers to specific questions regarding their distribution, diet, habitat requirements, and reproduction.

#### **1.2 Jeju Island**

Jeju Island is a typical volcanic island formed about 2 million years ago by a volcanic eruption. It is located in the most southerly portion of the Korean

**Figure 1.** G. ussuriensis *individual observed in Jeju Island.*

Peninsula. Its topography is smooth with an oval form extending in an eastnortheast direction [16]. There is a wide range of volcanic topographies. There are about 360 small volcanoes known as "Oreum". Oreums are distributed mainly in the middle mountain zones [17] that provide retreat sites for snakes. The highest peak on the island is 1950 m above sea level. Despite its small size (1833.2 km<sup>2</sup> ), a total of 830.94 km<sup>2</sup> (about 45%) land area was designated as a "Biosphere Reserve" by UNESCO (United Nations Education Scientific Cultural Organization) in 2002 [18].

The climate on Jeju Island is highly seasonal with cool, dry winters and warm, wet summers. The hottest month is August (average temperature of 26.5°C) and the coldest month is January (average temperature of 6°C). It contains various habitat types ranging from evergreen broadleaf forest, deciduous forest, and coniferous forest to grassland and wetland habitats [19]. The Island supports 4764 species of land flora [19]. Vertebrate species include 43 species of mammals (including sea mammals), 418 species of birds, 7 species of amphibians, and 14 species of reptiles [20].

### **2. Description**

#### **2.1 Morphology**

*G. ussuriensis* is a small-sized, highly venomous snake belonging to the family of Viperidae [21]. Its adults have short, moderately slender bodies not exceeding 650 mm (rarely more than 680 mm). Its tail length is 80 mm [22]. Males are generally larger than females (**Table 2**). The Head is large and often triangular because of the lateral projection of quadrate bones. Its very small eyes have typical vertical pupils with a fine bright edge. Its mouth has paired hollow fangs connected to venomous glands located behind the eye at the back upper part of the jaw. The tongue is pink or red and bifurcated. Scales are located in 21 rows on each side of the body. There are also abdominal scutes (16–66 pairs) and sub-caudal scutes (about 51 pairs).

The general ground color of the body is brown or brown of varying intensity, sometimes almost black. On the side of the body starting from the head, there is a row of elliptical or rounded dark spots with a light middle and darker edges. In the middle of the back, rings of opposite sides are often joined. The belly is yellow-gray with black marks anteriorly. In the central part, there is a combination of black and yellow-gray spots such that the snake is well camouflaged both in arboreal and terrestrial situations. Posteriorly, the belly is uniformly black. The melanistic individual from Jeju Island has been reported [24], with remarks on color variations of this species*.*


#### **Table 2.**

*Snout-vent length (SVL) comparison between male and female of* G. ussuriensis *in Jeju Island.*

*Ecology of Red-Tongue Viper (*Gloydius ussuriensis*) in Jeju Island, South Korea DOI: http://dx.doi.org/10.5772/intechopen.101277*

#### **3. Life history**

#### **3.1 Distribution**

*G. ussuriensis* is a species of a venomous snake having limited distribution worldwide. Currently, the known range of this species cover the following regions: Russian Far East, northwards to the lower Amur River, westwards to the Argun River, eastwards limited to the coast of the Sea of Japan and Tatarskiy Strait, the Korean peninsula, and northeastern China [21, 25]. In Korean Peninsula, it is commonly found in mainland South Korea, Jeju Island, and its associated islets. In Jeju Island, its distribution is homogenous (**Figure 2**) and it is one of the most commonly encountered snakes. In Jeju Island, it utilizes various habitats ranging from mountain forests to low altitude areas containing swamps and marshes [26, 27]. They are frequented more open microhabitats that had rocks or fallen logs that served as a refuge or basking spots. Agricultural land, grasslands, and freshwater streams are the areas of most frequent records. More commonly they were recorded from wetland sites adjacent to forested habitats as; Dongbaekdongsan, Muljangori, Mulyeongari, and Sumeunmulbaengdui wetland areas. Being hygrophilous, it is not uncommon on the sea. It is also recorded at an altitude up to 1947 m. However, until recently no information is available about population size.

**Figure 2.** *Distribution of* G. ussuriensis *in Jeju Island.*

#### **3.2 Habit and habitat**

Each species has its own unique behavior. Some spend most of the day foraging for food or basking in the sun, while others are most active at dusk and dawn or during the night. *G. ussuriensis* has plasticity in its diet, which allows this species to spread widely and survive in various landscape zones. Prey is identified by heat, followed by a sudden and rapid attack and bite. Basking in the sun is a common daytime activity in early summer. Hibernation begins from October to the middle of May of the following year. Each individual has its own hunting territory, beyond which it does not go. *G. ussuriensis* generally engages in limited movements. They may remain for long period in relatively small areas of approximately 64 m2 [28], where they can be repeatedly observed. They shed their skin from time to time during molting. Bites are excruciatingly painful, producing internal organ hemorrhages as well as bleeding at bite sites.

Most animals have their preferred habitats [29, 30], which may be influenced by species-specific temporal and spatial constraints. Vipers can live in different ecosystems including woodlands, forests, rocky areas, coasts, wetlands, swamps, mountainous regions, scrubs, and others. Habitat is an essential part of their survival and life history because it allows snakes to protect themselves from predators and it can be used for hibernation, breeding ground, and ambush. They can take refuge in burrows of rodents, among rocky slopes, boggy vegetation, and dense bushes. In Russia, *G. ussuriensis* usually adheres to forest edges, rocky taluses, abandoned settlements, ruins of old houses, and cemeteries. It is frequently observed on the coast of the Sea of Japan. In Jeju Island, it is common in cultivated land, low mountain areas, and forest areas. It can be seen hiding under stones. It is often found along banks of water bodies, dried-out ditches, and low-lying damp areas that provide more humidity. As a rule, it adheres to open space covered with grass or shrubs required for successful hibernation.

#### **3.3 Diet**

Every snake is zoophagous (consuming other creatures). All snakes are carnivorous. They eat animals, not vegetables. Some prefer specific prey, while others will eat just about everything they can grab and swallow. Snakes hunt different prey items, including rats, mice, rabbits, frogs, insects, lizards, other snakes, birds, bats, squirrels, and so on.

The diet of *G. ussuriensis* in its distribution range is not well documented. It has been stated that this species feeds primarily on frogs and other amphibians. They also feed on small mammals and other animals [31]. Thus, the diet of *G. ussuriensis* is typically broad. Kim and Oh [23] have studied prey items of *G. ussuriensis* in Jeju Island through manual palpation methods (**Figure 3**). Through the analysis of 177 individuals from 46 locations, a variety of prey items ranging from centipedes to amphibians, reptiles, and mammals were observed (**Table 3**). Among these prey, amphibians had the highest frequency of occurrence (55.2%), followed by mammals (20.7%), centipedes (13.8%), and reptiles (10.3%). The highest occurrence of the amphibian diet of *G. ussuriensis* is related to a higher abundance of herpetofauna at swampy (wetland) areas as good habitats of *G. ussuriensis* whose subsequent mimicry can kill the prey. The choice of prey differs in response to local and geographical variation in prey availability or abundance. At Gapado Island (Islets of Jeju Island, located 5.5 km off the Jeju coast), where prey items of *G. ussuriensis* were limited only to centipedes and lizards [23]. They concluded that the shift in diet was related to the lower density of favorable prey items.

*Ecology of Red-Tongue Viper (*Gloydius ussuriensis*) in Jeju Island, South Korea DOI: http://dx.doi.org/10.5772/intechopen.101277*

#### **Figure 3.**

*Prey detection of* G. ussuriensis *through manual palpation method.*


**Table 3.**

*Prey items of* G. ussuriensis *identified through manual palpation in Jeju Island.*

Head size and shape are not static, and however, most snake species have shown substantial flexibility in head shape [32, 33]. In a wide range of snakes, head form is surprisingly varied and has been hypothesized to be adaptive, with relative head width, in particular, is connected to the maximum prey size that may be eaten [34]. In general, larger snakes eat larger prey whereas smaller consumed smaller prey. In Jeju Island, a positive correlation was found between the size of the head of *G. ussuriensis* and the diameters of prey items [23].

#### **3.4 Reproduction**

Reproductive behaviors and rates vary drastically based on the species. Reproduction in snakes is controlled by the natural cycle of ambient warmth and cold [35] and red tongue vipers are no exception. Seasonal changes in light and rainfall, which impact food availability, might potentially play a role in reproduction for these ectotherms. Reproduction is dioecious. Mating takes place in April and May. The mating strategy of *G. ussurisensis* is not well documented yet but incidences of 2–3 males mating with a single female have been frequently observed (**Figure 4**).

#### **Figure 4.**

*The group mating of* G. ussuriensis *in Jeju Island. Two male and one female participating in group mating.*

However, one incidence of multiple males competing for a single female (forming mating ball) was observed within Jeju Island (personal communication). Like other members of the viper family, *G. ussuriensis* is ovoviviparous. They retain eggs inside their bodies until they hatch and give "live" birth.

Much like other snake species, [36] red tongue viper reproduce annually. In Jeju Island, seasonal cycles based on size and histological examination of testes and follicles in ovaries have been reported by Kim and Oh [23]. The change in the monthly average value of the Testis Index (TI) was large between June and July. It was relatively stable between July and August, while it was the largest between August and early September (**Figure 5**). The average length of the largest follicle in a female's ovary was at its largest in May and smallest in June (**Figure 6**). After intensive vitellogenesis in May, ovulation and fertilization seem to occur since June. Most births occur between the end of August and September when females give birth to 2–10 offspring in one brood.

Newborn babies completely repeat the color of their parents. With the analysis of 146 newborns, the mean weight of neonates was 4.3 ± 0.7 g (range, 1.1 g–6.6 g) and the mean length (NS) of neonates was 174.3 ± 12.6 mm (range, 110–203 mm). They reach sexual maturity at a body length of 400 mm, possibly after the second or third hibernation. Before hibernation, newborn snakes have time to molt 5–6

#### **Figure 5.**

*Monthly pattern of male testis index. Cross line represent means and horizontal lines represent standard deviation.*

*Ecology of Red-Tongue Viper (*Gloydius ussuriensis*) in Jeju Island, South Korea DOI: http://dx.doi.org/10.5772/intechopen.101277*

#### **Figure 6.**

*Annual pattern of ovarian largest follicle length in female* G. ussuriensis *in Jeju Island. Horizontal thick lines represent means and horizontal thin lines and vertical bars represent standard deviation and ranges.*

times. The first molt occurs after 6–7 h and the second molt occurs after 2–3 days. At first, newborns feed on insects and invertebrates. Later, they switch to normal food. Life expectancy on average ranges from 9 years to 15 years. In captivity, this may increase.

Adult females of many snake species breed on a less-than-annual basis, indicating the requirement of a long foraging period to accumulate sufficient reserve for offspring production [37]. *G. ussuriensis* females have a one-year breeding cycle [23]. According to indirect data, in the north of Primorsky and the Khabarovsk Territory in Russia, this species may have a two-year breeding cycle. Depending on factors such as prey densities and favorable weather conditions, some degree of synchrony is observed during clutch or litter production by females within a population.

#### **3.5 Natural predators and competitors**

*G. ussuriensis* members, particularly young ones, have someone to fear. They are frequently attacked by birds of prey (hawk, white-tailed eagle, and black kite), large-billed crow and jay, and predatory mammals (badger, Siberian weasel). Competition from other vipers does not seem to be occurring in Jeju Island. In many parts of the world, humans hunt vipers for food [38]. The genus Gloydius, has long been known for its medicinal value in Asia. Dried *G. ussuriensis* meat is eaten for medical treatment by inhabitants of Japan and Korea. Thus, hunting for them has made people their main enemy.

#### **4. Threat**

#### **4.1 Habitat loss and fragmentation**

The most serious risks to biodiversity are habitat loss and fragmentation. It is reasonable to believe that habitat loss and fragmentation will be the most serious dangers to snake populations worldwide [39, 40]. Where the natural forest is destroyed and replaced with intensive agriculture, coniferous plantations, or urban development, *G. ussuriensis* faces a particularly serious threat. Such changes will definitely have a detrimental effect on the prey abundance of snake species, decreasing predators' chances of long-term survival [41].

As vehicle ownership and traffic levels increase, many new roads are being built everywhere in Jeju Island, with a greater proportion of them being broad, fast highways. Snakes usually travel a certain distance in search of a mate and seek nesting sites, which force them to cross roadways. As a result, many individuals are killed on the roads. Some others interact with threats such as humans, farm equipment, vehicles, and pets (dogs and cats), which put *G. ussuriensis* populations at serious risk.

#### **4.2 Introduction of invasive species**

Invasive species frequently have immediate and widespread detrimental consequences for populations, natural groups, and biodiversity [42]. The impact of invasive alien species on native snakes species in the world has been recorded, including the introduction of Cane Toad (*Thinella marina*) in Australia [43], Indian Mangoose (*Herpestes javanicus*) in some Antillean Islands [44], and three species of fire ants (*Solenopsis invicta, S.geminata,* and *Wasmannia auropunctata*) in Africa and New-Zealand [45].

In 2017, a red fire ant (*S. invicta*) was discovered in South Korea. Since then, it has subsequently spread to various states within the country [46]. This species is of high concern because it has caused severe damage to many aspects of human life and wildlife [47] due to its aggressiveness and toxicity [48, 49]. Quantitative evaluation of climate suitability of the invasive red fire ant suggests that this ant has a high possibility of settlement after its introduction in Jeju Island [50]. Invasive red fire ants have the potential to harm *G. ussuriensis* indirectly through their negative effects on their prey and directly by predation facilitated by their potent stings.

#### **4.3 Human persecution**

The persecution of snakes by humans is widespread, especially among venomous snakes. Many snakes are killed regardless of whether they are venomous because people tend to have an irrational fear of these creatures. *G. ussueriensis* is often intentionally killed by hikers and hunters, although such an act is considered illegal. Building new roads can bring more people to formerly inaccessible places, increasing the danger of snakes being killed as a result of misinformation. Even experienced field biologists have limited knowledge of this snake's behavior and biology. It is difficult to establish a positive public perception of poisonous snakes. However, an adequate legislative framework can alleviate such issues. It is essential to educate people about the importance of snakes to modify their attitudes regarding venomous snakes.

#### **5. Conclusion**

*G. ussuriensis* is the most widespread species in Jeju Island and has suffered greatly, due to habitat loss, fragmentation, and increased mortality from roads and human persecution. The ecology of *G. ussuriensis* in Jeju Island was studied which aids in understanding the general biology of the species. *G. ussuriensis* is the smallsized, highly venomous viperidae having widespread distribution within Jeju Island. *Ecology of Red-Tongue Viper (*Gloydius ussuriensis*) in Jeju Island, South Korea DOI: http://dx.doi.org/10.5772/intechopen.101277*

Through the manual palpation method, *G. ussuriensis* was identified in consuming amphibian, centipede, reptiles, and mammals. Being dioecious, mating takes place in April and May and gives birth to live young's toward the end of August and September. A complete understanding of ecology could help in implementing the conservation and management plans. Increasing people's knowledge and understanding about snake and snakebite treatment and prevention through educational interventions like snake parks and snake museums is a low-cost method to promote a snake-friendly mindset.

Here, we attempt to provide useful knowledge to locals, scientists, and conservation agencies. Because this field is in its infancy, we are forced to rely heavily on results published in other languages, personal communication, and results of unpublished experiments. We believe that successful initiatives, even if limited in their impact are informative and might well prove broadly applicable for snake conservation.

#### **Acknowledgements**

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2019R1A6A1A10072987).

#### **Appendices and nomenclature**


#### **Author details**

Hong-Shik Oh1 \* and Maniram Banjade2

1 Interdisciplinary Graduate Programme in Advance Convergence Technology and Science, Faculty of Science Education, Jeju National University, Jeju, South Korea

2 Practical Translational Research Center, Jeju National University, Jeju-Si, South Korea

\*Address all correspondence to: sciedu@jejunu.ac.kr

© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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[45] Holway DA, Lach L, Suarez AV, et al. The causes and consequences of ant invasions. Annual Reveiw Ecology, Evolution and Systematics. 2002;**33**:181-233

[46] Lyu DP, Lee HS. The red imported fire ant, solenopsis invicta buren (hymenoptera: formicidae: myrmicinae) discovered in Busan sea port, Korea. Korean Journal of Applied Entomology. 2017;**56**:437-438

[47] Vinson B. Invasion of the red imported fire ant (hymenoptera:

formicidae): Spread, biology and impact. American Entomology. 1997;**43**:23-39

[48] Jemal A, Hugh-jones M. A review of the red imported fire ant (*Solenopsis invicta Buren*) and its impacts on plant, animal, and human health. Preventive Veterinary Medicine. 1993;**17**:19-32

[49] Solley GO, Vanderwoude C, Knight GK. Anaphylaxis due to red imported fire ant sting. The Medical Journal of Australia. 2002;**176**:521-523

[50] Byeon D, Lee J, Lee H, et al. Prediction of spatiotemporal invasive risk by the red imported fire ant (hymenoptera: formicidae) in South Korea. Agronomy. 2020;**10**:1-15

#### **Chapter 5**

## Comparative Ecology of Two Species of Semiaquatic Snakes in Southeastern North America

*Jeffrey D. Camper*

#### **Abstract**

The banded water snake (*Nerodia fasciata fasciata*) and the Eastern cottonmouth (*Agkistrodon piscivorus piscivorus*) were the focal species in a long-term mark and recapture study in the upper coastal plain of South Carolina, USA. Recapture rates were low for both species. Female *N. fasciata* were significantly larger than males. Male *A. piscivorus* were larger than females but not significantly. Age structure and sex ratios were determined for these populations. Recapture latency was greater for *A. piscivorus* than for *N. fasciata.* There was little dietary niche overlap between these two species. *Nerodia fasciata* ingested significantly more fish headfirst and more amphibians tail first. Growth rates were also calculated for both species. Litter size, offspring size, relative clutch mass and parturition dates were determined for *N. fasciata.*

**Keywords:** banded water snake, Eastern cottonmouth, reproduction, food habits, population ecology, sexual dimorphism

#### **1. Introduction**

Certain aspects of the life history of an organism can have important fitness consequences [1]. Snakes have lagged behind other groups of vertebrates in the understanding of life history traits due to difficulties in detection and sampling [2]. Successful reproduction is the primary measure of fitness but life history parameters such as foraging success, thermoregulation and habitat choice are important to survival and therefore a prerequisite to fitness increases [3, 4]. In an attempt to elucidate the importance of these ecological factors I studied two semiaquatic snake species on the coastal plain of southeastern North America.

The banded water snake (*Nerodia fasciata*) is a moderate sized (to 1524 mm total length) heavy bodied snake with a dorsal color pattern of brown to reddish-brown bands with grayish to brown pigment between the bands [5] (**Figure 1**). The labial scales bear dark bars at their margins and a dark stripe runs from the eye to the angle of the jaw. Larger specimens frequently lose much of the banding and are uniformly brown. This species occurs throughout the coastal plain of southeastern North America from the state of North Carolina south to Florida and west to Texas [6]. It can be found in almost any body of fresh water including streams, rivers, lakes, ponds, marshes, sloughs, canals and swamps. Life history data for this species has been summarized by [5, 6].

#### **Figure 1.**

*Adult female banded water snake (Nerodia fasciata fasciata) from the study site. Note faint bands in upper left part of photograph.*

The cottonmouth or water moccasin (*Agkistrodon piscivorus*) is a large (to 1890 mm total length) pitviper with a thick brown stripe on the side of the head that runs through the eye to the angle of the jaw (**Figure 2**). Pale lines both above and below border this stripe. The large triangular shaped head is distinctly wider than the neck and the pupil is vertically elliptical. The dorsal color pattern consists of wide dark brown bands with lighter centers that alternate with a lighter brown ground color. Many larger specimens have the banding pattern obscured and appear a uniform dark brown. The inside of the mouth is lined with white tissue and is used

#### **Figure 2.**

*Adult male Eastern cottonmouth (Agkistrodon piscivorus piscivorus) from Clarendon County, South Carolina, USA. Note the gaping behavior that inspires the common name.*

*Comparative Ecology of Two Species of Semiaquatic Snakes in Southeastern North America DOI: http://dx.doi.org/10.5772/intechopen.101574*

as a warning to potential predators [7]. Cottonmouths occur in many of the same habitats as banded water snakes [6]. One long term mark recapture study was published by [8] for a western population of this species. Other aspects of the biology of this species have been reviewed by [6, 9].

The objective of this long-term study was to compare the ecology of syntopic populations of these semiaquatic snakes that are distantly related and from different clades [10]. *Agkistrodon piscivorus* and *Nerodia fasciata* show striking similarities and marked differences in many of their life history traits [5, 6]. Both are live bearing but differ in that *Nerodia* are income breeders with larger litters of smaller offspring whereas *Agkistrodon* are capital breeders producing small litters of larger young [11]. Female water snakes usually breed annually whereas female cottonmouths do not. Even though both species consume similar prey they employ different foraging behaviors. *Nerodia* are active foragers whereas *A. piscivorus* use sit and wait or ambush foraging [5, 12].

#### **2. Methods**

#### **2.1 Study site**

The study site was the Pee Dee Research and Education Center (PDREC), a 972 ha experimental agricultural facility owned by Clemson University, located in the upper coastal plain of Darlington County, South Carolina, USA. A series of six ponds formed by damming a creek was sampled most intensively (**Figure 3B**), a larger pond nearby was also sampled (**Figure 3A**), and Back Swamp (**Figure 3C**) an undammed creek north of the other two sites was sampled as well. All three of these wetlands flow east into Dargan's Pond which is a man-made reservoir. The ponds were surrounded by mowed grass, old field or strips of woody vegetation consisting of alder (*Alnus* sp.), willow (*Salix* sp.), loblolly pine (*Pinus taeda*), bald cypress (*Taxodium distichum*), sweet gum (*Liquidamber styraciflua*) and oaks (*Quercus* sp.). The swamp contained riparian forest which includes the above-mentioned woody plants plus red maple (*Acer rubrum*), water tupelo (*Nyssa aquatica*) and tulip poplar (*Liriodendron tulipifera*). The littoral zone of all wetlands consisted of emergent vegetation that included water lilies (*Nuphar* sp., *Nymphaea* sp.), smart weed (*Polygonum* sp.), bur-reed (*Sparganium* sp.) and patches of penny wort (*Hydrocotyle* sp.). The climate of this region consists of hot humid summers (mean June–August high temperatures during 2002–2006 were 33°C) [13]. Precipitation averaged 14.5 cm per month during June–August 2002–2006 and the region has mild winters with the mean January high temperatures of 14°C during 2002–2006.

#### **2.2 Data acquisition**

Snakes were sampled most frequently using double ended funnel traps although opportunistic hand captures under artificial cover objects placed along the shoreline or on or near roads were used as well. Commercially available metal minnow traps (Cuba Specialty Manufacturing Co., Filmore, NY, USA) 42 × 22 cm, plastic funnel traps (model 700; N.A.S. Incorporated, Marblehead, Ohio, USA), vinyl coated wire funnel traps (Academy Sports + Outdoors) and funnel traps made from hardware cloth that were 41 × 22 cm with 5 cm funnel openings [14] were used to sample *Nerodia fasciata* and *Agkistrodon piscivorus.* Pre-manufactured metal traps had their funnel openings enlarged to approximately 3 cm with a rake handle. Traps were placed about 3 m apart in shallow water (water depth < trap diameter) along logs, in emergent vegetation and along short aluminum drift fences. The drift

#### **Figure 3.**

*The Pee Dee Research and Education Center, Darlington County, South Carolina, USA. The property boundaries are outlined in black. (A) Pond near headquarters, (B) ponds where most data were collected, (C) back swamp. The Great Pee Dee River is on the upper right just outside the property boundaries. The scale bar in the lower left is 800 m.*

fences consisted of 5 m lengths of aluminum flashing oriented perpendicular to the shoreline with two traps placed at each end. Due to low capture rates, 0.007 captures/trap day (1 trap day = one trap out over 1 night, hereafter TD) in 1998 to 0.011 captures/TD in 2002, traps were checked at 48 h intervals and were either disabled or not checked on weekends when PDREC was closed. From 2010 onward traps were checked daily and closed over weekends.

Sampling took place from 1998 to 2003, 2010–2011, 2014 and 2016. Data collection from *A. piscivorus* was not started until August 1999. Sampling occurred from July–October 1998 (960 TD), May–October 1999 (4108 TD), May–July 2000 (994 TD), April–June 2001 and 2002 (810, 994 TD respectively), and May–June 2003 (757 TD) [15]. Starting in 2010 multiple shorter sampling periods per season were introduced following the robust design of [16]. Sampling occurred for 7 days in March, 11 days in April, 9 days in May–June, 9 days in August and 14 days in September during 2010. In 2011 sampling occurred for 10 days in each of May and June. During 2014 snakes were sampled for 10 days in May, 6 days in June and 5 days in September. During 2016 sampling occurred for 7 days in May and 10 days in each of June and August. The number of traps used ranged from 97 to 140. From 2010 to 2016 trapping effort ranged from 665 to 1876 TD per trapping period.

Snakes were usually processed in the field. Snout to vent length (hereafter SVL) and tail length (TL) was measured to the nearest mm with a measuring tape for *Nerodia* and a squeeze box [17] was used to measure SVL, TL, head length and head width of

#### *Comparative Ecology of Two Species of Semiaquatic Snakes in Southeastern North America DOI: http://dx.doi.org/10.5772/intechopen.101574*

*A. piscivorus*. The squeeze box was a modified plastic toolbox 66 cm × 28 cm × 28 cm. Head length and width were measured to the nearest 0.1 mm with calipers for *N. fasciata*. Mass was measured with Pesola spring scales to the nearest 1 g. Except for *Nerodia* neonates, snakes were marked with passive integrated transponder (PIT) tags [18]. Newborn *Nerodia* were marked by clipping ventral scales [19]. Sex was determined by examination of the base of the tail or by probing the tail. Data were taken from recaptures only after a minimum of 14 days had elapsed since the previous capture.

Diets were studied by examining stomach contents. Prey were palpated from the stomachs of *Nerodia* and stomach contents were recovered from cloth bags or from traps for both species. Only prey from traps with evidence of ingestion (saliva, mucous, envenomation) were included in the analyses. Prey mass was measured to the nearest 0.1 g using an electronic balance. Prey length and width were measured to the nearest 0.1 mm with calipers. Prey were identified to species when possible. Prey availability was measured by counting all prey in all traps during one day of most sampling periods. Prey counts were conducted in May and August of 2010, May of 2011, May and September of 2014 and May, June, and August of 2016 (**Table 1**). Dietary niche overlap used the formula of [20].

Females were palpated for embryos when processed. In 1999 four gravid *N. fasciata* were kept in the lab until parturition. Pregnant females were given water and food ad libitum. Food consisted of frozen/thawed fish purchased alive from a bait store. Pregnant snakes were kept on a 12:12 light: dark cycle at approximately 27°C. One died about 1 week prior to giving birth. Young were weighed and measured and marked by scale clipping. They were released at the site of maternal capture. Clutch sizes were also reported from oviductal eggs of females that died in traps. Cloacal swabs were taken from both sexes of each species from 1999 to 2001 to look for the presence of sperm. The ductus deferens of one male of each species were also examined for the presence of sperm.

Growth rates were calculated from recaptures as the difference in SVL in mm divided by the number of days between captures. The active season was considered 15 April through 15 October which is 183 days per year. Even if active the animals were considered to not be feeding and therefore not growing before 15 April or after 15 October. Negative growth values were not used in calculating growth rates and were considered the result of measurement error.

#### **2.3 Statistical analyses**

Tests for normality utilized the Shapiro-Wilks test and visual examination of box plots and histograms. Homoscedasticity was examined using the F-test or Bartlett's test.


#### **Table 1.**

*Prey availability in one pond where most snakes were sampled in this study. Numbers are percentages. See text for explanation of methods.*

Due to correlation among response variables (mass, SVL, TL, head length, head width), a multivariate analysis of variance (MANOVA) was used to test for sexual differences. The Welch t-test was used to test differences between individual variables due to unequal variances. Means are followed by ±1 standard deviation (SD) and an α ≤ 0.05 is considered significant in all statistical tests. Statistical analyses were performed in R version 4.1.1 [21]. Due to heteroscedasticity some data were natural log transformed.

### **3. Results**

#### **3.1 Population structure**

A total of 181 *N. fasciata* and 93 *A. piscivorus* were marked in this study. Because year was used as the sampling period in the early part of this study (1998–2003) and shorter periods during the latter part of the study (2010–2016) estimates of

#### **Figure 4.**

*Size distribution of captures of each sex of (A) Nerodia fasciata; (B) Agkistrodon piscivorus at the Pee Dee Research and Education Center, Darlington County, South Carolina, USA. The ordinate is the number of captures.*

*Comparative Ecology of Two Species of Semiaquatic Snakes in Southeastern North America DOI: http://dx.doi.org/10.5772/intechopen.101574*

population size and survivorship could not be calculated. Recapture rates were higher for *N. fasciata* (31.5%) than for *A. piscivorus* (16%). Few neonates were captured with only 1.66% of the sample for banded water snakes and 6.45% for the cottonmouths. Subadults were defined as >1 year old but not sexually mature and made up a larger part of the sample for both species with 27% for *Nerodia* and 25.8% for *Agkistrodon*. **Figure 4A** indicates that most male *N. fasciata* were between 350 and 550 mm SVL whereas most adult females were between 550 and 750 mm SVL. There was a peak in adult female *A. piscivorus* from 600 to 750 mm SVL (**Figure 4B**). Captures of both sexes of *Nerodia* peaked in May and females showed a smaller peak in August (**Figure 5A**). Male captures gradually declined throughout the summer. Low numbers for July were due to lower trapping effort. Adult male cottonmouth captures peaked in May and declined throughout the summer (**Figure 5B**). Female captures peaked in June and showed a smaller peak in September. Sex ratios exhibited a female bias and were 1.4F:1M for each species. However, four litters of *N. fasciata* born in the lab had sex ratios that did not differ from 1:1 (*X*<sup>2</sup> = 4.934, df = 3, p = 0.084839).

**Figure 5.**

*Seasonal distribution of captures of (A) Nerodia fasciata; (B) Agkistrodon piscivorus at the Pee Dee Research and Education Center, Darlington County, South Carolina, USA. The ordinate is the number of captures.*

Recapture latency or the time between captures in days for each species was calculated based upon an activity season from 25 March to 10 November which is 231 days per year. Mean days between captures for male *N. fasciata* were 116.5 ± 193.6 days (range 2–814 days) and for females it was 60.4 ± 58.1 days (range 4–233 days). These were not significantly different using a two-sample t-test with unequal variances (t = −0.334, df = 23, p = 0.7415). Mean recapture latency for both sexes combined was 80.7 ± 126.1 days (range 2–814 days). Mean recapture latency for *A. piscivorus* was 263.3 ± 575.4 days with a range of 12–2074 days. Although recapture latency was greater for *A. piscivorus* the difference was not significant (t = −1.7025, df = 15.295, p = 0.1089) with a two-sample t-test with unequal variances.

#### **3.2 Sexual dimorphism**

*Nerodia fasciata* and *Agkistrodon piscivorus* exhibit different patterns of sexual size dimorphism. Females are larger in *N. fasciata* whereas males are larger in *A. piscivorus* (**Table 2**). A multivariate analysis of variance (MANOVA) showed significant differences between the sexes for *N. fasciata* (Pillais' trace = 0.340, F (1, 140) = 14.002, p < 0.001) for the morphological variables in **Table 2** but not for *A. piscivorus* (Pillais' trace = 0.117, F (1, 86) = 2.17, p = 0.065). Female *N. fasciata* were significantly greater in mass (t = 3.5508, p = 0.0005), SVL (t = 3.983, p = 0.0001), head length (t = 5.025, p < 0.001) and head width (t = 5.218, p < 0.001). However, tail length was not significantly different (t = 1.6743, p = 0.0963) between males and females. Relative tail length (tail length/total length; hereafter RTL) was greater for males of both species. For *N. fasciata* mean male RTL = 0.262 ± 0.016 (0.197–0.286, N = 55) whereas females averaged 0.241 ± 0.014 (0.197–0.269, N = 87). Values


#### **Table 2.**

*Sexual dimorphism in body and head size of adult Nerodia fasciata and Agkistrodon piscivorus from South Carolina, USA. Numbers are means ±1 standard deviation.*

for male *A. piscivorus* were 0.159 ± 0.019 (0.111–0.229, N = 33) and for females 0.153 ± 0.016 (0.110–0.197, N = 56). The sexual dichromatism with males retaining a bolder banding pattern was also observed in this population of *A. piscivorus* [22].

#### **3.3 Growth rates**

Growth rate estimates were available for 28 *N. fasciata* and 6 *A. piscivorus*. Growth rates (mean ± 1 SD) were 0.726 ± 0.626 mm/day (0–2.3 mm/day) for *N. fasciata* and 0.783 ± 1.26 mm/day (0.029–3.31 mm/day) for *A. piscivorus*. Mean female *N. fasciata* growth rates were almost twice that of males (female 0.824 ± 0.672 mm/ day, 0–2.3 mm/day, N = 21; male 0.432 ± 0.353, 1–1.029 mm/day, N = 7). Small sample size precluded statistical analysis. One female *A. piscivorus* that was originally marked on 3 May 2001 was recaptured on 28 April 2010 and had grown only 52 mm in almost 9 years and had a growth rate of 0.0322 mm/day.

#### **3.4 Food habits**

Both species fed frequently upon fishes whereas banded water snakes ate amphibians frequently but not reptiles and cottonmouths consumed reptiles but few amphibians (**Table 3**). The number of prey per stomach ranged from 1 to 8 for *N. fasciata* and 1–5 for *A. piscivorus*. Multiple prey were found in 10 of 24 (41.7%) banded water snakes and 3 of 5 (60%) cottonmouths. One 715 mm SVL female *A. piscivorus* contained 1 catfish, 1 sunfish (*Lepomis* sp.), 1 pickerel (*Esox* sp.), 1 frog (*Lithobates* sp.) and one Eastern musk turtle (*Sternotherus odoratus*). All but the turtle was swallowed headfirst. Mass ratios (prey mass/snake mass) given as mean ± 1 standard deviation followed by the range was greater for *A. piscivorus* (0.159 ± 0.208, 0.186–0.526) than for *N. fasciata* (0.109 ± 0.083, 0.0096–0.3889). Banded water snake stomach contents were 44% fishes and 56% amphibians whereas cottonmouth stomach contents were 46% fishes, 50% reptiles and 4% amphibians. Only one *N. fasciata,* a female 380 mm SVL, had eaten one Eastern mosquito fish (*Gambusia holbrooki*). Larval anurans made up the largest proportion of amphibians, with metamorphosed anurans contributing 18.7% and salamanders only 1.7% of the total. The dietary niche overlap [20] was low between these two species (O = 0.01024). Only *A. piscivorus* more than 550 mm SVL included reptiles in their diets and *N. fasciata* over 750 mm SVL dropped amphibians from their diets. Banded water snakes did not swallow prey headfirst more frequently than tail first (*X*<sup>2</sup> = 0.34, df = 1, p > 0.05) however, fishes were swallowed headfirst significantly more often, and amphibians tail first (2 × 2 contingency table, *X*<sup>2</sup> = 17.049, df = 1, p < 0.05). Small sample sizes precluded statistical analysis of *A. piscivorus* stomach contents.

Prey availability was assessed by counting all potential prey in the traps during one day per sampling period. There were eight prey censuses during this study (**Table 1**). Crayfish decreased in abundance during the season. Fishes and amphibians varied between sampling dates but did not show any discernible trends. *Gambusia holbrooki* made up a mean of 11.13 ± 7.73% (1.6–23.7%) of the samples.

#### **3.5 Reproduction**

The smallest male *N. fasciata* with sperm in the cloaca was 397 mm SVL and was sampled on 24 September 1999. Because a specimen 395 mm SVL sampled on 28 June 1999 lacked cloacal sperm, 400 mm SVL was designated as adult size for male *N. fasciata*. Eight males contained sperm (397–600 mm SVL) and 8 others (320–655 mm SVL) did not. Two males with sperm were from May, 4 from June


**Table 3.**

*Frequency of occurrence of prey found in 25 Nerodia fasciata and 14 Agkistrodon piscivorus from the Pee Dee Research and Education Center, Darlington County, South Carolina, USA. N is the number of prey items in the sample.*

and 2 from September. The males lacking sperm included 4 from May, 1 from June, 2 from July and 1 from August. The smallest male *A. piscivorus* that had sperm in the ductus deferens was 500 mm SVL and was caught on 26 May 2000. Another male (863 mm SVL) had cloacal sperm on 23 May. Three males lacking sperm were 768–961 mm SVL and were sampled in May (2) and July.

The smallest gravid female *N. fasciata* was 575 mm SVL however 500 mm SVL was used as the size for sexual maturity in analyses [23]. In 2000 92% of females were gravid and 91% in 2006 indicating that most females probably reproduce

*Comparative Ecology of Two Species of Semiaquatic Snakes in Southeastern North America DOI: http://dx.doi.org/10.5772/intechopen.101574*

annually in this population. Only 58% of female *A. piscivorus* were gravid in 2000 indicating a likely biennial reproduction in females of this species. The smallest gravid female *A. piscivorus* was 660 mm SVL and 500 mm SVL was used as minimum adult size for females of this species as well [24]. During 1999 four gravid *N. fasciata* were brought into the lab until parturition. One specimen died on 13 August with embryos in developmental stage 36 [25]. Clutch sizes ranged from 12 to 28 (mean ± 1 SD) was 18.45 ± 5.24 (N = 11). There was a significant positive correlation between maternal SVL and clutch size (r = 0.723, p = 0.018, N = 10). Dates of parturition for females that gave birth in the lab were 5 and 23 August and 3 September. The earliest in the season that females were found to be pregnant was 17 May for *N. fasciata* and 18 May for *A. piscivorus*. Relative clutch mass (RCM) ranged from 0.19–0.478 (mean ± 1 SD) was 0.335 ± 0.119 (N = 4). Mean neonate mass from three litters born in the lab was 3.89 ± 0.51 g (3–5 g, N = 66) and the mean SVL for these same snakes was 153.72 ± 5.77 mm (133–166, N = 66). Data on size of oviductal eggs came from four females collected in late May and early June which were at a similar enough developmental stage to be lumped into a single data set. Mean oviductal egg length was 21.30 ± 5.01 mm (13.2–32.7 mm, N = 66 ova) and mean oviductal egg width for the same ova was 13.82 ± 3.99 mm (7.7–19.9 mm, N = 66). One 715 mm SVL *A. piscivorus* collected on 26 May 2000 contained five oviductal eggs with a mean length of 35.68 ± 1.63 mm (33.9–37.5 mm) and a mean width of 21.94 ± 0.82 mm (21.0–22.9 mm). Three *N. fasciata* with oviductal eggs had more in the right oviduct than in the left. Mean (± 1SD) for the right oviduct was 10.33 ± 1.15 (9–11) and for the left 7 ± 1 (6–8) but not significantly more (*X*<sup>2</sup> = 1.924, df 1, p > 0.05). No banded water snakes had more in the left oviduct and the one *A. piscivorus* had two in the right oviduct and three in the left.

Stub tails and body scars can give information on potential predation pressure on snakes [26]. Nineteen male *N. fasciata* exhibited stub tails (15) or body scarring (4) which was 35% of the sample. Female *N. fasciata* showed 37.6% injured snakes with 26 of 32 with stub tails and 6 with body scarring. Cottonmouths showed a much lower frequency of injuries with only 4 of 32 males (12.5%) showing injuries and only one with body scarring. Females had the same numbers of injuries which showed an 8.3% injury rate.

#### **4. Discussion**

#### **4.1 Population structure**

Because population sizes and survival rates could not be estimated the discussion of population structure will focus on age structure and sex ratios. Only 3 neonate *N. fasciata* and 6 neonate *A. piscivorus* were caught in this study. Under sampling of juvenile snakes is usually attributed to low survival rates [27] however it may also be from trapping bias as neonatal snakes can escape through the mesh of traps [28] which I think may have occurred in this study for *N. fasciata.* Neonatal *A. piscivorus* are too large to escape through the trap mesh. Captures of subadult snakes, defined as >1 year old but not sexually mature, were frequent for both species (**Figure 4**). This finding may indicate these populations have a relatively young age structure and therefor may be undergoing population growth [29].

Sex ratios for both species were skewed in favor of females which I think may be due to sampling bias. Primary sex ratios were not different from unity for *N. fasciata*. There was a secondary peak of captures of postparturent females in August (**Figure 4**). Sometimes the same females were caught in the same traps on consecutive days (J. Camper, unpublished observation) as found by [30] in another South

Carolina population. Female capture bias was shown by [31] for both focal species in Texas. In another study in Texas, using a different sampling method, [8] found a sex ratio not significantly different from one for *A. piscivorus*. Three other populations of this species were found to have slight male bias [22, 32, 33] as did one study of *N. fasciata* in another region of South Carolina [32].

#### **4.2 Sexual dimorphism**

I found that female *N. fasciata* were significantly greater in mass, SVL and head size than males whereas tail length was not significantly different. Similar results were found in another South Carolina *N. fasciata* population located about 180 km southwest of my study site [32]. The latter study did not examine head size, however. Patterns of sexual dimorphism in *A. piscivorus* contrasted with *N. fasciata* but were not statistically significant and in agreement with [22, 34]. Although head size was not significantly different between the sexes of cottonmouths [33] found that males had longer quadrate bones than females. The males in this population retain a bold banding pattern similar to juveniles that was first documented by [22]. Relative tail length averaged about 2% longer in males of *N. fasciata* but less than 1% longer in *A. piscivorus.* Similar findings for both species were published by [35] for specimens collected from throughout North Carolina. The values reported here were higher for *Nerodia* but close to those of *Agkistrodon* calculated by [34].

#### **4.3 Growth rates**

Growth rates have not been reported for *N. fasciata* so they will be compared to the closely related *Nerodia sipedon* [10]. Growth rates from this population were higher than the 0.12 mm/day mean for male and the 0.14 mm/day mean for female *N. sipedon* in Lake Erie [26]. The *N. sipedon* study was from a northern population with a much shorter growing season which could affect growth rates. Three neonate *N. fasciata* caught in August (1 snake) and September (2) averaged 173.67 ± 16.29 mm SVL. This was 20 mm longer than the mean for lab born snakes suggesting that growth may occur before their first winter. Cottonmouth growth rates reported here were also higher than reported for western populations of 0.210–0.280 mm/day [24] and 0.170–0.434 mm/day [8]. Because male *N. fasciata* mature at about 400 mm SVL (see below) they may reach sexual maturity by the end of their second year and mate the following spring. Females probably mature 1 year later when they surpass 500 mm SVL. Based upon these growth rates, male *A. piscivorus* may reach sexual maturity in about 2.5 years and females in about 4 years.

#### **4.4 Food habits**

These two species exhibited little dietary niche overlap which was probably due to *A. piscivorus* having few amphibians and many reptiles in its diet. The banded water snake diet documented in this population is similar to that found in other populations [5, 36] except that *G. holbrooki* was consumed only once by one juvenile banded water snake. In a study in Louisiana *N. fasciata* consumed 30.6% *G*. *holbrooki* and 11.2% amphibians [37]. *Nerodia fasciata* may be avoiding *G. holbrooki* at this study site because it appears to be an abundant species at this locality and only one specimen was found in the stomach contents. Banded water snakes ingested significantly more fish headfirst. This could be due to scales covering the fish. Snakes feeding on reptiles usually swallow prey headfirst and scales are used in prey orientation [38, 39]. *Agkistrodon piscivorus* is known for its broad diet that includes mammals, birds and their eggs, alligators and pit vipers in addition

#### *Comparative Ecology of Two Species of Semiaquatic Snakes in Southeastern North America DOI: http://dx.doi.org/10.5772/intechopen.101574*

to what was found in this study [6, 40]. Five different species of amphibians were found in North Carolina specimens [35]. There is geographic variation in the diet of this species also, as evidenced by [41] finding no amphibians in the diet to amphibians making a large proportion of the diet in other populations [24, 33]. No novel prey were found in the diet of *A. piscivorus* in this study but the lesser siren (*Siren intermedia*) is a newly documented prey species for *N. fasciata.* Larger mass ratios for *A. piscivorus* as compared to *N. fasciata* was not surprising given that the former have relatively larger heads and a greater gape [33].

Frequencies of stub tails and body scarring were more than 20% higher in *N. fasciata* than in *A. piscivorus* at my study site. Injury frequency may reflect predation intensity or predator efficiency [26]. I believe the former to be true in this study because of the relatively high frequency in *N. fasciata* and the lower frequency in *A. piscivorus*. Because the latter is a large pit viper with potent venom it probably experiences less predation pressure than *N. fasciata*. Injury frequency was about 15% higher for *N. fasciata* in this study when compared to another population about 180 km to the southwest [34].

#### **4.5 Reproduction**

Litter sizes documented here agree with what has been found in other populations of both species [24, 32, 35, 41–46]. The correlation of maternal SVL and litter size is well documented in snakes [47] and was found for another South Carolina population of *N. fasciata* [32]. The RCM found in this study is larger than the 0.201 reported for one specimen of *N. fasciata* [48]. Parturition dates for *N. fasciata* were like those in other populations [43, 45]. Neonate sizes reported here averaged 4 mm SVL longer than reported by [28] for another South Carolina population. Three neonates trapped in August and September were small enough to escape through the trap mesh [28]. The mean SVL for 6 neonate *A. piscivorus* trapped in this study was 277.67 ± 56.46 (215–344) which is larger than reported for other populations [8, 24, 42] but smaller than neonates from Florida [49]. The low proportion of pregnant female *A. piscivorus* found here suggests that females give birth biennially in this population. Most populations of cottonmouths reproduce biennially [8, 24, 49, 50]. However, some populations may have annual reproduction [23, 42]. All three gravid female banded water snakes had more ova in the right oviduct which was also reported by [51] for one Texas specimen. More embryos in the right oviduct of *A. piscivorus* were also reported by [44, 46] unlike what was found here.

#### **5. Conclusions**

Two common snake species, the banded water snake (*Nerodia fasciata*) and the Eastern cottonmouth (*Agkistrodon piscivorus*) were studied on the coastal plain of southeastern North America. This long-term mark-recapture study used funnel traps to sample the snakes. Approximately 180 *N. fasciata* and 93 *A. piscivorus* were marked in this study. Recapture frequencies were low and population size estimates and survival rates could not be calculated.

Sexual size dimorphism favors females in *N. fasciata* which were significantly larger in mass, SVL and head size than males. Males were the larger sex for *A. piscivorus* but this was not significant. Growth rates were 0.726 ± 0.626 mm/day (0–2.3 mm/day) for *N. fasciata* and 0.783 ± 1.26 mm/day (0.029–3.31 mm/day) for *A. piscivorus*. Both species exhibited female biased secondary sex ratios which may be due to sampling bias. Primary sex ratios of four litters of *N. fasciata* were not significantly different from one.

Male *N. fasciata* reach sexual maturity at about 400 mm SVL and females at about 500 mm SVL. Males may be able to reach this length in about 2 years and females in 3 years. Male *A. piscivorus* reach maturity at 450 to 500 mm SVL which takes about 3 years. Female *A. piscivorus* mature at about 500 to 550 mm SVL which probably takes 3–4 years.

Both species fed upon fish and *N. fasciata* included many amphibians in its diet whereas *A. piscivorus* ate reptiles but few amphibians. Fish prey were swallowed headfirst and amphibian prey usually tail first. Female banded water snakes appear to breed annually whereas female cottonmouths probably breed every other year. Clutch sizes ranged from 12 to 28 with a mean of 18.45 ± 5.24 (N = 11) for *N. fasciata*. There was a significant positive correlation between maternal SVL and clutch size. One female *A. piscivorus* contained 5 oviductal eggs. Clearly more work is needed on these populations to determine population size estimates, survivorship and to elucidate the reproductive biology of *A. piscivorus.*

#### **Acknowledgements**

Funding was provided by Francis Marion University (FMU) and the South Carolina Governor's School of Science and Mathematics (GSSM). The administration of the Pee Dee Research and Education Center graciously provided access to the property. The South Carolina Department of Natural Resources provided scientific collecting permits. Jason Doll helped with statistical analysis. Numerous FMU students helped with field work including J.R. Burger, L.D. Chick, A. Crawford, M.P. Grooms, R. Hanson, T. Hardymon, M. Jaco, T. Jensen, A. MacNeil, B. Reid, H. Sellers, and T. Tedder. GSSM students M. Blew, M. Chandler and M. Patel also aided in field work. Ben Camper helped in the field as well. This research benefitted greatly by discussions with J.D. Willson.

#### **Author details**

Jeffrey D. Camper Department of Biology, Francis Marion University, Florence, South Carolina, USA

\*Address all correspondence to: jcamper@fmarion.edu

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Comparative Ecology of Two Species of Semiaquatic Snakes in Southeastern North America DOI: http://dx.doi.org/10.5772/intechopen.101574*

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