Nutritional Choice and Diet Diversity
Of
Sika Deer (Cervus nippon taiouanus)
In the Tropical Forest of Taiwan


INTRODUCTION

To understand the food selection of herbivores, both aspects of optimal nutritional requirements and food diversity are essential. Freeland & Janzen (1974) did a nutritional hypothetical work and demonstrate how herbivores avoided the toxic secondary compounds in their daily diet. Pyke et al. (1977) also applied a mathematical model to predict the optimization of dietary choices. However, there is a great need for certain detailed empirical studies about specific nutrient distribution in plant communities which herbivores selected as food, and how they adjust the nutritional optimization to satisfy the other important consideration, such as the need of reproduction and physically growth seasonally. In this paper, the optimization approach is adopted to assess the daily and seasonal nutritive need in the deer's diet. This nutritional model deals with the seasonal strategy of food plant selection of Sika Deer (Cervus nippon) in Taiwan.
Ruminated ungulates favor different food plants to maximize the net intake of protein and energy. For example, moose were found to be "energy maximizers" (Belovsky 1978). Formosan Sika deer, a generalist herbivore, inhabit the lowland plain (0-300 meters in altitude) of the tropical forest in Kenting, Taiwan. The area is full of a variety of trees, shrubs and grass, where the strong wind effect leads to crimping vines and wind-tolerant shrubs occupying the patchy rock areas, and forming a unique food reserve. Formosan Sika Deer adopted a relatively flexible strategy to browse the forage plants in different terrain and maintained a dynamic relationship with the vegetation (Hu & Wang 1994). In this field study, the different plant intake amount by deer and its specific nutrition intake spectrum (protein and energy) were examined. It was also determined whether the real food preference was consistent with the optimal foraging theory (Schoener 1971, Stephen & Krebs 1985), and the empirical data explored in what degree the deer optimize its dietary choice to balance the nutrition demands and resource constraints.
This research summarized the food selection principle and the foraging behavior of Sika deer in South Taiwan peninsula based on a nutritive optimization model, which will contribute to the conservation plan of this endangered species and ecosystem management in the future. This paper focused on nutritional analysis of food plants to understand how nutritive choices achieved the physiological requirement seasonally. In addition to the nutrient analysis in lab and field observation, this study also explored how the nutritive diversity and its changes over time supported the seasonal needs of the deer population.

METHODS AND EMPIRICAL DATA

Data

The data in this research was collected in Area I (fig 5) of Sheting Natural Park, Kenting National Park, Taiwan from April 1993 to Sept. 1994. Of the deer in this area, there were 2 males and 4 females, which were radio-collared by S6 type activity transmitters (Telonics Co.). Receivers and H-shaped antenna were used to track the radio signal and follow the deer. Two collared male deer (Y42 and B6) and one sympatric female deer group (B2 and its female group, including 3 females and 3 fawns) were found easily to approach. This population was targeted to observe the detailed nutritive intake intensively in a 10-hectare area. I observed their food habits and foraging behavior from a relatively close distance (within 3 meters) with binoculars (Bushnell, 8x30). While locating the targeted deer, I recorded its behavior and food items every half minute. The sampling methods depended upon individual and specific behavior: in male deer, a focal sampling alone per hald minute was adopted; in female group, a scan sampling consistently recorded each deer (Lehner 1979; Martin 1986, Hu et al. 1994). The food plants selections were identified and the intake amount was estimated by multiplying intake time with average intake
(g/min.) for that plant in a lab cafeteria test. Each month we observed 3-6 days in the daytime (range from 6 a.m. to 6 p.m.). Totally we recorded the deer 47 days over 1.5 years, and 184 feeding hours excluding resting intervals.

Study Area
Kenting National Park at the southernmost tip of Taiwan, Henchun peninsula. The reintroduction park is a 120-hectare area and located at Sheting beside the Pacific Ocean. The altitude ranges between 100 and 200 meters, and there are low hills and a number of uplifted coral reefs scattering around the park. The north of Area I where the targeted population lived has two short streams flowing northwest to southeast. The seasonal streams in wet season and underground flow in dry season have a dramatic difference in flow to influence the water source for wildlife and moisture retention.
The climate is subtropical with a rainy season and typhoons in summer; mean rainfall exceeds 1900 mm during May-Sept. per year and annual rainfall averages about 2200 mm (Central Weather Bureau, Taipei, Taiwan). About 90% of rainfall is during the wet season (May-Sept.); and there is severe drought in the dry season (Oct.-April) since the evaporation rate is higher than the precipitation rate.
The vegetation of this whole area is seasonal forest, and is represented by a mosaic of grassland, shrub, and Acacia forest. The early migration cultivation and the long-term browsing effect of cattle in the pasture resulted in the formation of the patchy habitats. Of the whole area, the most area was occupied by dominant vegetation, such as semi-deciduous forest, Acacia forest on the hill slope and evergreen sclero-phyllous forest upon reef rock. Under the canopy, there are scattered native plants (e.g. Acanthus & Verbena) with the invaded exotic legume (Leucaena glauca). The territory of the focus deer population within Area I was approximately 10 hectares, which included several ponds, a field climate station, and an abandoned house, which was utilized by deer as shelter.

Nutritional Analysis and Intake Calculation
To calculate the daily intake amount of protein and energy, I used the general standard equations of total nutrient intake (Hudson & White 1991). The net protein and energy intake amount can be written as:

p_total = p1+p2+p3+...

c_total = c1+c2+c3+... (1)

where P is the daily total intake amount of protein (g/day), C is the daily total intake amount of energy (calorie/day); Pi is daily protein intake amount (g/day) contributed from a specific plant species i, Ci is daily energy intake (cal/day) contributed from the plant species i; ti is the observed feeding time (in minutes) for plant i; ri is the feeding rate (g/min) for that food plant, which was indirectly measured in the short-term captive periods of wild population (n=43 in Area I) by providing the natural food and observing its intake condition to estimate the foraging consumption rate in lab in June 1993.
To evaluate the food quality and its nutritive values, we conducted a test for 49 plants of primary food items and dominant vegetation species. Energy (cal/g), protein (%), and ADF (acid detergent fiber, %) for certain forage plants were sampled in summer (August 1993) and winter (February 1994) respectively. The nutritive examinations were done by the nutrition analysis lab in the National Husbandry Examination Center, Tainan, Taiwan. In equation (1), pi is the protein concentration (%, g of protein/total-g) and ci is the energy concentration (calorie/g) for each specific food plants, which information was obtained from the above nutritional analysis lab (Table 1).

Step 1. The basic nutritional values (protein [p] and energy [c])
Within limited budget, we tested both favorable and unfavorable food plants as many as possible (table 1). I denoted each plant an identification code starting with its vegetation group: A(tree), C(vine), D(shrub), E(herb) and F(grass). Totally we obtained the protein values (% in weight base) for 33 plants (fig 10), and energy content (kcal/kg) for 22 plants (fig 9). When we separated those plants dichotomously with natural gap (fig 7), we got a direct sense some plants were important in nutrition, some not (table 6).

Step 2. Conduct a monthly behavioral observation about the foraging time (min.) toward each plant (Ti value)
Kuo (1994) studied the same deer population and obtained informative data for total foraging time. He found out there was no significant difference in activity pattern between day and night. I only observed the foraging behavior in day time, but calculated an estimated average foraging time for a particular plant per day. I also extracted the feeding (including walking, searching and intaking) and true intake ratio from my observations (table 5).

Step 3. Consider seasonal time constraint (T*)
Kuo (1994) estimated a daily foraging ratio of 24 hours, which changed over seasons. Generally seasonal time constraint (T*) ranged from 14.3% (rut period in male deer) to 50.6% (wet season) of 24 hours. By integrating step 2 & 3, we estimated how many minutes deer feed on a specific plant per day (table 4).

Step 4. Physical intake rate (r) determines the nutrient intake rate (a,b) partially
Our model didn't deal with the protein and energy concentration (p,c) directly. However, we need to know the specific nutrient intake rate: a (g/min.) is protein intake rate and b (kcal/min.) is energy intake rate , which are equal to physical foraging rate times nutrient values (p,c) (see equation 1 & 2). If we lacked information of the certain plant's physical intake rate (r), we just extrapolated and referred the value from the same vegetation group to make it up.

Step 5. Is the comparison of two-plants model appropriate and effective?
To keep this model simple, there is an assumption by comparing the top two plants to represent the major nutritive intake source of deer, where we calculate the fitness function and make judgements. The result demonstrated: the plant species a1 always showed up in the primary food list (table 5), except 4 months in total 40 monthly observations. The ratios occupied by the top two plants ranged from 25.4% to 70.7% per observation. If we calculated frequency that foraged 40+% intake from the top-2-plant system, there were 82.5% (37/40) observations available and it seemed effective enough to give us some sense of food selection behavior: Sika deer usually focused on a limited number of important plants to compose their daily diets (table 5).

Step 6. Broad diet spectrum vs. specific major food
Our model only considers the main resource of nutritive intake, especially limited in protein and energy. However, there are a lot of reasons deer don't favor some high-nutritional food, for example plants a15, a33, d1 and d18 (fig 12). The possible reasons might depend on our incomplete knowledge of wildlife about digestive mechanism and rumen toxicology (see discussion). By eliminating some doubtable toxic food plants (which were not favorable for deer, e.g. d1, d18, a33), we focused on a reasonable set with a series of nutritive values (fig 8).

Step 7. Identify the plant a1 as the yearly primary food
Since major food plants have to be abundant enough to contribute to the daily diet, we only compare the relationship between the primary food (a1) and other submajor food in step 5 list (e1, a4. f1). Even though we don't know exactly how parameters of fitness function behaves, and nutritive constraint values (P*,C*), we can compare the intake amount (estimated by the foraging time) to test the model prediction: will deer always choose the plant with better protein and energy? The scatter plots (fig 13,14,15) show us a clear tendency: plant a1 wins! To somewhat degree, deer foraged plant a1 heavily, discarding which plant was the other submajor food. The extent of clusters by feeding on plant a1 varied over seasons.

RESULTS
Exotic Plant (a1) as a Rich-Nutrient Deer Food

Plant a1 (Leucaena glauca (L.) Benth.) is an exotic legume from South America, which was introduced into Taiwan for fuel and paper pulp. After World War II, this species was no longer of economic interest and neutralized in secondary forest and disturbed land in South Taiwan, where the climate was similar to its native habitat. This legume has a better nitrogen-fixing ability due to its symbiotic rhizo-bacteria in the root system. Both in dry and wet seasons, the legume a1 became the most favorable deer food due to its excellent nutritional characteristics, including nutrient concentrations of protein and energy (p,c) and the respondent intake rates (a,b) (fig 8, table 1).
Plant a1 was the primary source of food plant yearly for the Sika deer to obtain both protein and energy, which appeared in the primary food list (90% occurrence, only 4 observation records didn't show up as a major food, table 4) and led deer spent a significant time to search and feed it. Since deer could intake enough nutrients through feeding a1, the predominant exotic species, the deer also chose a variety of submajor food plants to meet the other physiological and favorable requirements (table 5), and maximized the fitness, growth rate, survivorship or fecundity. To summarize the major (a1) and submajor forage plants, the deer spent most of their daily feeding time to intake these 2-3 primary species (table 5). In this case, our two-plant diet model can properly work with 80% of the Sika deer data, which a1 and the other submajor plants contributed to the most forage amount daily (39.5-70.7%).
According to our simple model theoretically, it implies the deer would spend much more time in foraging plant a1 as a nutrition optimal choice, rather than considering e1, a4, and f1, which all are secondarily important food sources. While the deer focused on searching and feeding a1 or e1 (fig 13 for e1) as the daily major food, the relative intake amount by foraging from a4 and f1 were significant low (fig 14 for a4, fig 15 for f1).

What's Going with the Widespread and Exotic Plant A1 and Recovery Sika Deer?
If the recovery deer population can adapt this widespread and exotic plant well as a qualified food, deer will take advantage in the invaded lowland patches (lower than 300 meters elevation) without a serious concern about the limit of food supply. Excluding the basic nutritional requirement, we still need to check the other factors of carrying capacity and deer conservation, such as the balance of minor elements, human population density, habitat fragmentation, dispersal corridor and land use in human-dominant ecosystem. We need an integrated program to combine all useful information to assess the potential habitat in the short-coming future.

Food Habit
This research included 151 food plant species from 62 families, including 5 species of pteridophyte, 116 species of dicotyledon and 30 species of monocotyledon. That deer fed proportionally more on woody species than herbaceous species (Chi-square, p<0.05) indicated that deer at Sheting area tended to be browsers, rather than grazers.

Nutritive Change between Summer and Winter
We observed the favorable and unfavorable forage plants by deer browsing, and analyzed their nutritional contents (Table 2). In tropical Taiwan, the hot and humid summer is the growth season for deer and plants. Generally speaking, the quality and quantity of forage plants match the physiological needs of Sika deer synchronously.
1. In nutrient content of heat energy, most summer forages were better than winter forages. The only exceptions were a4 and e1.
2. In protein concentration, most summer forages were better than winter forages. There were exceptions of a1, a6 and d1.
3. ADF method is to estimate lignified nitrogen, lignin and cellulose by extracting plant tissue with strong acid solutions. ADF method is also widely used as an easy method to measure the fiber in a feed (Van Soest 1982). In ADF testing, the plants in early autumn (Aug.1993) had more fiber content than spring (Feb.1994).

Nutritive Diversity of Forage Plants
The preference and intake amount of the forage plant primarily reflect its nutritive values and the anti-herbivore mechanisms with either physical or chemical agents. Some rich-nutrition plants were not browsed by deer due to its strong taste and toxic components, such as a33 & d18 (table 2). I also listed the relative secondary compounds which had significant amount in plant to detect.
1. The rich-energy forages were a33 (unfavorable acacia, predominant vegetation), d1 (unfavorable citrus, native fence tree), a1 (much favorable, especially leaf and fruit, exotic and neutralized legume as fodder plant), a15 (unfavorable mahogany, native fence tree), and d18 (unfavorable verbena, shelter shrub). The poor-energy forages were a4 (favorable mulberry) and c14 (favorable in specific season) (Fig 9).
2. The rich-protein forages were a1 (much favorable legume), a33 (unfavorable acacia), d18 (unfavorable verbena), a41(unfavorable sandalwood), and d1 (unfavorable citrus). The poor-protein forages included grasses (f1, f2) (Fig 10).
3. The rich-fiber (ADF) forages were e49 (unfavorable agave, exotic fiber plant as cable raw material in World War II), c9 (favorable spurge vine), e38 (unfavorable lily), a15 (unfavorable mahogany), and grasses (f1, f2). The poor-fiber forages were a1 (very favorable legume), a4 (favorable mulberry), a6 (favorable loquat) and c17 (favorable dog bane) (Fig 11).
4. Most plants in our survey had energy content from 3.6-4.2 kcal/kg, and protein content from 7-15% (Fig 12).

DISCUSSION

Nutritional Change over Time
Nutrition of deer forages varies with the physiological state and development of forage plants. Even though seasonal change of nutrients in tropical Taiwan was not obvious, we deduced that new growth in early summer had more protein content than the matured leaves in winter, because the young leaves accumulated protein in protoplasm to grow. In winter or dry season, forage tended to have low nutritive value. In summer or wet season, the forage yield was at its maximum, and the nutritive values were higher. In fall, the leaves predominated with hydrolysis, which lignified the cell wall and increased fiber, so the ADF value increased in August.

Nutritive Diversity in Plants to Fulfill the Foraging Need
Forage quality or digestibility varies between plants, seasons, and locations (Klein 1962). The effective factors are climate (light, temperature, moisture), soil quality, species variation, and terrain difference (exposure, altitude, slope). There was a positive correlation between nitrogen (protein) content of forages and their nutritive quality, while a negative correlation exists between fiber content and nutritive quality. Both nitrogen (protein) and fiber are reliable indicators of forage quality (Klein 1965). Basically, the deer most favorite forages tended to have higher energy or protein, and have less fiber content. On the other hand, the unfavorable forages tended to more fiber which the deer avoided. We found, for some reason, deer didn't feed on the rich-nutrient (energy or protein) forages as we supposed. Those plants had a somewhat strong taste (e.g. d1, a15, a41) or certain defensive substances (e.g. d18, a33)(table 3).

Defensive Substances as an Anti-Herbivore Mechanism
The resisting substances of plants include lignin, cutin, and many secondary compounds. The function of those substances is to resist wind, disease, and herbivore's browsing. They reduce the nutritive value of the forage plant (Van Soest 1982), and avoid deer's over-browsing as to reserve the essential resource for plant growth and reproduction.
Secondary compounds, such as alkaloids, glycosides, saponins, tannin, terpenes, phenols, etc., have a clear defensive rather than metabolic role. They have a metabolic source and are often stored in fresh and vulnerable tissues that are not defended by physical structures like lignins and silica. Secondary compounds may always have a greater effect on browsers (e.g. Sika Deer in Kenting) than grazers, because of its high concentration and local distribution in plant parts (Table 2). For example, wood plants and vines tend to be more highly defended towards browsers. (Bryant 1991)

About the secondary compounds:
1. Alkaloids
Alkaloids are the heterocyclic nitrogenous compounds that exhibit the inhibitory activity towards digestion. In our study area, there were certain rich-alkaloid plants: a1 (much favorable), a23 (favorable), and d18 (unfavorable). Although d18 (verbena) also had better protein and energy, but deer seemed to merely treat it as a shelter plant and didn't feed on it. Sometimes the specific d18 fruit attracted deer to browse, but deer always were careful not to forage the other parts. We believed the reason might be its high level of alkaloids, glycosides and saponins. We do not understand how the deer's digestive system is able to absorb nutrients with high alkaloid contents, such as plant a1 and a23.

2. Essential Oils
Essential oils represent a diverse group of organic substances in plants that are volatile and soluble in organic solvents. They have low molecular weight such as ester, ether, phenols and terpenes and also exhibit antimicrobial activity. When those plants are browsed, rumen organisms would change or make some adjustments (Schwart 1980).
Legume (e.g. a1) is the essential forage for deer either in captivity or in the wild. Legume also has terpenoid throughout the plant body, which includes saponins and steroids (table 2) and would be somewhat toxic, although rumen bacteria might have ability to partially detoxify them. Some terpenoids also have potential to cause stable foam formation and to promote RBC hemolysis (Van Soest 1982).
We observed that deer primarily fed on a1 legume either in dry or wet seasons, and obtained high energy and protein contents from this quality forage. Deer may regulate the intake amount with different feeding patterns and behavioral controls to avoid its overdosed terpenoids toxicity.

3. Tannin
Tannin may be effective as toxins, rather than a defensive compound by its protein precipitating ability (Robbins 1987). Because of the high content of tannin in a33 (acacia), Sika Deer didn't browse this predominant vegetative plant even though it was high in energy and protein contents. In addition, other forages with more or less tannin content might be browsed in a limited dose (a23, d3), or the deer would avoid tasting the highly protective plant parts with tannin, such as a1 bark and a6 fruit (table 3).


Literature Cited

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Table 2. Plant List and the Examination of Nutritive Contents
(Nutritive test date: S=summer samples in Aug. 1993; W=winter samples in Feb. 1994)

ID scientific names test browsing common
of forage plant date amount name

Tr
a1. Leucaena glauca (L.) Benth. (leaf, fruit) W,S ++++ legume
a2. Macaranga tanarius (L.) Muell.-Arg. W,S +++ spurge
a3. Pittosporum pentandrum (Blanco) Merr. W,S ++ (Pittosporaceae)
a4. Broussonetia papyrifera (L.) L'Herit. ex Vent. W,S +++ mulberry
a6. Eriobotrya deflexa (Hemsl.) Nakai W,S ++ rose - loquat
a8. Trema orientalis (L.) Blume W,S + elm
a15. Aglaia formosana (Hayata) Hayata W - mahogany
a23. Terminalis catappa L. W ++ (Combrefaceae)
a31. Ficus wightiana Wall. ex Benth. W + mulberry - ficus
a33. Acacia confusa Merr. W - legume - acacia
a41. Champereia manillana (Blume) Merr. W + sandalwood
a43. Bambusa dolichoclada Hayata W + bamboo
Vines
c1. Ipomoea obscura (L.) Ker-Gawl. W +++ morning glory
c3. Passiflora suberosa L. W,S ++ passionflower
c4. Trachelospermum gracilipes Hook. f. W ++ dos bane
c7. Gymnema alternifolium (Lour.) Merr. W +++ milkweed
c9. Mallotus repandus (Willd.) Muell.-Arg. W ++ spurge
c12. Merremia gemella (Burm. f.) Hall. f. W ++ morning glory
c14. Piper kawakamii Hayata W,S + (Piperaceae)
c15. Parsonia laevigata (Moon) Alston W + dog bane
c17. Trachelospermum jasminoides (Lindl.) LemaireW + dog bane
Shrubs
d1. Murraya paniculata (L.) Jack. W,S - rue / citrus
d3. Ardisia cornudentata Mez W + (Myrsinaceae)
d4. Pandanus odoratissimus L. f.
var. sinensis (Warb.) Kanehira W + (Pandanaceae)
d18. Lantana camara L. W - verbena
d28. Hibiscus taiwanensis Hu W - mallow
Herbs
e1. Hypoestes cumingiana Benth. & Hook. W,S ++++ acanthus
e2. Stachytarpheta jamaicensis (L.) Vahl. W + verbena
e38. Ophiopogon formosanum Ohwi W + lily
e47. Lygodium japonicum (Thunb.) Sw. W ++ fern (Schizaeaceae)
e49. Agave sisalana Perr. ex Enghlm. W + agave
e51. Cyperus alternifolius L.
subsp. flabelliformis (Rottb.) KukenthalW + sedge
Grasses
f1. Miscanthus floridulus (Labill.) Warb.
ex Schum. & Laut. W,S +++ grass
f2. Imperata cylindrica (L.) Beauv.
var. major(Nees)Hubb.ex Hubb. & VaughanW,S ++ grass


Table 3. Distributions of second compounds in deer forage plants in Taiwan
(substance distributions in plant parts: lf=leaf, fr=fruit, sd=seed, bk=bark,al=all plant, rt=root, st=stem)

ID (second compounds class) distributed parts - specific substances, local concentration (if available)

Trees
a1 (alkaloids)lf,fr-mimosine, leucenol (saponins)lf sd-sitosterol4.6% (tannin)bk6.25% sd lf
a3 (saponins)al-hederagenin,barrigenol (tannin)al 0.4% al-edergenin
a6 (glycosides)lf,sd-amygdalin1.4% (saponins)lf sd (tannin)lf fr 0.17% (others)
lf-As 0.012%(fresh);0.022%(old) fr-pectin 1.03% sd-HCN 0.004% fr-Na, K 0.22%, Fe 0.02%
a23 (alkaloids)al,fr-trigonelline (tannin)al bk 6.26% rt 7.77% (others)al-Mg(much), K(rare,3.87%) al-phytosterol fr-glucosazon, pentosan al-pyridine 0.1%(K salt, etc)
a31 (glycosides)lf-flavonic glycoside, coumarin (others)rt,st-phenoid
a33 (tannin)al:5-16%(age=10-30 yr)
Vines
c1 (glycosides)sd-pharbitin 2.0%, gibberellin glucoside 7%
c3 (others)al-theine, leucodelphinidin
c4 (glycosides)al (others)al-acetamide, inositol dimethyl ether,arctin
c7 (others)al-sarcostin,metaplexigenin,benzoylramanone,deacylcynanchogenin,utendin,pergularin,lanoxin
c14 (others)al-piperidine, piperidene, futoenone, futoxide
c17 (glycosides)al-flaronglycoside (others)al-lanoxin, tracheloside, acetamide, inositol dimethyl ether
Shrubs
d1 (others)bk-mexoticinlf-isopentyl limettin, exoticin, heptamethoxy flavone, cadinene, flavone, coumarin, engenol, imperatorin, murralogin, meranzin, imurrangatin, noracrolnlcine
d3 (tannin)al (others)al-bergennin, querectin, myricitrin
d4 (others)lf-phenol
d18 (alkaloids)al (glycosides)al-lanoxin (saponins)al (others)al-flavoid
d28 (glycosides)fl-anthocyanin,f lavonic glycoside
Herbs
e2 (glycosides)al (others)al-phenol 0.0028%
e47 (others)al-phenol
Grass
f2 (glycosides)al (others)al- K 0.75%