Oecologia (1995) 104:297-300 �9 Springer-Verlag 1995

John F. Wilmshurst �9 John M. Fryxell

Patch selection by red deer in relation to energy and protein intake: a re-evaluation of Langvatn and Hanley's (1993) results

Received: 10 October 1994 / Accepted: 27 May 1995

Abstract Langvatn and Hanley (1993) recently reported that patch use by red deer (Cervus elaphus) was more strongly correlated with short term rates of intake of di- gestible protein than dry matter. Such short term mea- sures overlook effects of gut filling, which may constrain intake by ruminants over longer time scales (i.e., daily rates of gain). We reanalyzed Langvatn and Hanley's da- ta using an energy intake model incorporating such a processing constraint, to determine whether their conclu- sions are robust. We found that the use of patches by red deer was just as strongly correlated with an estimate of the daily rate of intake of digestible energy as one of di- gestible protein during four out of seven trials, but slight- ly lower in three out of seven trials. In all cases, daily in- take of digestible energy was a much better predictor of patch preference by red deer than was the intake of dry matter. Our reanalysis suggests that the daily intake of energy was highly correlated with that of protein in these trials, as may often be the case for herbivores feeding on graminoids. Hence the observed pattern of patch use by red deer could simultaneously enhance rates of both pro- tein and energy intake.

Key words Energy �9 Cervus elaphus �9 Foraging �9 Patch selection �9 Protein

Introduction

Langvatn and Hanley (1993) recently reported on an ele- gant experimental study of the evolutionary basis for patch selection by red deer (Cervus elaphus). In their ex- periment, captive red deer were permitted to select among 16 large patches of timothy (Phleum pretense) maintained at four different levels of biomass. They

J.E Wilmshurst �9 J.M. Fryxell (~) Department of Zoology, University of Guelph, Guelph, Ontario, N1G 2W1, Canada Ph: 519-824-4120 ext. 3630 Fax: 519-767-1656 e-mail: jfryxell@uoguelph.ca

compared the time spent in each patch with estimated rates of intake of digestible protein (DP) and digestible dry matter (DDM) within those patches. Their results clearly showed that patch use by red deer was more strongly correlated with short term rates of intake of pro- tein than of dry matter.

Langvatn and Hanley (1993) stated that their experi- mental results do not conclusively demonstrate the basis for patch selection by red deer. Indeed, they argued that protein was a better indicator than digestible dry matter largely because protein was a more sensitive index of plant phenological stage and therefore plant quality. Nonetheless, some naive readers might be tempted to conclude from Langvatn and Hanley's results that dry matter or energy gain are unimportant currencies in red deer foraging strategies.

A substantial body of research suggests that daily rates of intake by herbivores are ultimately constrained by rates of processing and clearance of ingesta through the gut (Amann et al. 1973; Belovsky 1978; Mould and Robbins 1982; Doucet and Fryxell 1993; Fryxell et al. 1994). If rates of digestive processing change with matu- ration stage of the vegetation, due to changes in fiber or lignin content, than short term rates may give a mislead- ing impression about the benefits of feeding in a patch of given biomass.

In this paper we reanalyze Langvatn and Hanley's (1993) data using an energy intake model that predicts daily rates of energy intake for grazing ruminants (Fryx- ell 1991), using experimentally determined parameters for Cervus elaphus (Wilmshurst et al. 1995). We show that Langvatn and Hanley's (1993) results are consistent with maximization of daily intake of both protein and energy, after taking into account the effect of plant phenological stage on digestive passage rates. The latter possibility was briefly mentioned by Langvatn and Han- ley, but they were not in a position to consider its poten- tial implications. We also explain why short term mea- sures of digestible dry matter intake may be poor predic- tors of patch use.

298 OECOLOGIA 104 (1995) �9 Springer-Verlag

Mater ia ls and methods

The model

In this reanalysis, we are concerned exclusively with predicting daily energy gain from measures of herbivore dry matter intake and forage quality. The general model we use was described in de- tail by Fryxelt (1991), with subsequent elaboration and application by Wilmshurst et al. (1995) to Cervus elaphus in North America. The model is based on the premise that there is a fundamental trade-off between the availability of grass and its rate of process- ing by ruminants.

The availability constraint is modelled as the product of the functional response and forage digestible energy (DE) content, where the functional response is an increasing function of grass biomass (Wickstrom et al. 1984; Gross et al. 1993; Wilmshurst et al. 1995). Hence, this constraint should increase monotonically over the range of grass biomasses considered in Langvatn and Hanley's (1993) experiments.

The processing constraint is modelled as ad libitum intake multiplied by forage DE content. Given that passage rate limits in- take (Arnold 1985) and passage is slow for poor quality forage (Van Soest 1982), the digestive constraint should decrease with in- creasing grass biomass (Ammann et al. 1973; Mould and Robbins 1982). The minimum of these functions with slopes of opposite signs dictates the daily rate of energy intake. The model generally predicts that the daily rate of energy gain should often be maxi- mized for ruminants at low to intermediate forage biomass (Fryx- el1 1991; Wilmshurst et al. 1995).

Data analysis

We incorporated Langvatn and Hanley's (1993) data into our mod- el to estimate the daily rate of energy gain for red deer feeding on patches of timothy of various biomass levels. We assume an aver- age body mass of 106 kg for red deer and an energy density for timothy of 19.25 kJ/g (Mellin et al. 1962; Armstrong 1964).

To estimate forage DE content, we multiplied Langvatn and Han- ley's (1993) DDM values by a regression formula relating forage DDM to DE for wapiti (Cervus elaphus nelsoni; Mould and Robbins 1982). This value was multiplied by the functional response used by Langvatn and Hanley (1993) in their estimate of dry matter intake (Wickstrom et al. 1984) to estimate the availability constraint. To es- timate the processing constraint we multiplied the DE function by ad libitum intake values for wapiti (Mould and Robbins 1982). Foraging costs were taken from wapiti bioenergetic data (Gates and Hudson 1978; Wickstrom et al. 1984) scaled to red deer body size.

The daily rate of energy intake was calculated for various bio- mass levels of timothy, over the range 0-6000 kg/ha. We followed Langvatn and Hanley's (1993) methodology in using the magni- tude of r 2 values (Casella 1983; Myers 1986) to evaluate the alter- nate hypotheses that patch use by red deer was proportional to (1) daily energy intake, (2) short term protein intake or (3) short term dry matter intake.

Table 1 R 2 values relating the goodness-of-fit between observed red deer patch use and predicted patch use taken from Langvatn and Hanley (1993) (L & H) and calculated by us (W & F). Nota- tion corresponds to that of Langvatn and Hanley (1993). H o pre- dicts patch use of a model forager moving among patches random-

Results

Langva tn and H a n l e y ' s (1993) data suggest that DE de- c l ined l inear ly wi th increas ing b iomass (kg/ha) (y = 67 .6-0 .003x, F1,24 = 81.5, P < 0.001, r 2 = 0.77). Mul t ip ly ing this by the funct ional response gave an in- creas ing avai labi l i ty constraint , and mul t ip ly ing by ad l ib i tum intake gave a decreas ing process ing constraint . This resul ted in a d o m e - s h a p e d in take funct ion (Fig. 1), the shape o f which suggests that red deer should max i - mize their da i ly rate o f energy gain when feeding in grass swards with a b iomass o f 930 kg/ha. We used this funct ion to es t imate the da i ly rate of energy gain by red deer for each exper imenta l patch and trial repor ted by Langva tn and Hanley (1993).

In all trials, patch use was more s t rongly corre la ted with da i ly energy gain than D D M intake (Table 1). In four of seven trials, there was jus t as s trong a corre la t ion be tween patch use and the da i ly rate o f energy gain as prote in gain (Table 1). In three of seven trials, however , the corre la t ion be tween patch use and pro te in gain was s l ight ly h igher than that of energy gain. To evaluate the degree o f s imi lar i ty be tween our es t imates of dai ly rates o f energy in take and Langva tn and Han ley ' s (1993) esti- mates o f D D M and D P intake, we ca lcula ted Pearson corre la t ion coeff ic ients (1"). Da i ly rates o f energy intake were more s t rongly corre la ted with short t e rm prote in in-

141

Z m

>.

re DJ Z UJ F- UJ Z

9 0

6 0

3 0

i i

~ 2 4 6 F O R A G E B I O M A S S

Fig. 1 Function predicting daily net energy intake (kJ day -1 kg body mass ~) for red deer over a range of vegetation densities (kg/ha x 103). Daily net energy intake is maximized at 930 kg/ha

ly, H2a predicts patch use of a forager matching time in patch with digestible protein intake, H2b predicts patch use of a forager matching time in patch with digestible dry matter intake and DE predicts patch use of a forager matching time in patch with daily net energy intake

Hypothesis Trial number

1 2 3 4 5 6 7

L & H, H o 0.384 0.531 0.521 0.532 0.555 0.651 0.515 L & H, H2a 0.941 0.946 0.952 0.841 0.863 0.888 0.739 L & H, H2b 0.211 0.045 - 0.158 0.451 0.599 0.455 W & F, DE 0.671 0.591 0.758 0.876 0.933 0.877 0.736

take (r 2 = 0.79) than short term rates of dry matter intake (r 2 = 0.49), presumably because protein content covaried with digestible energy content. Hence, it is not surprising that both measures had similar predictive power.

Discussion

Our reanalysis of Langvatn and Hanley's data, incorpo- rating a model with a digestive constraint on daily food intake, suggests that patch use by red deer may be just as strongly correlated with daily rates of energy intake as short term rates of protein intake. At the very least, our results show that estimated DE intake is a much better predictor of patch use than DDM intake.

Of course, it is always possible in science that none of the alternate hypotheses under consideration explain the pattern of interest. In this case, there are certainly viable alternate hypotheses that have not been explicitly consid- ered. For example, one could postulate (as did one of our anonymous reviewers) that red deer simply choose the youngest plants available, on the grounds that immature plants often have the lowest level of fiber, as well as the highest levels of soluble nitrogen and protein [e.g. Lang- vatn and Hanley's (1993) Figs. 3, 4]. The plant quality hypothesis is inconsistent, however, with Langvatn and Hanley's (1993) observations.

Langvatn and Hanley's (1993) protocol involved four grass treatments, comprising different planting dates. At the beginning of the foraging experiment, grasses in treatment I had grown undisturbed for 1 year, treatment II for 5 weeks, treatment III for 3 weeks, and treatment IV for less than 1 week. Accordingly, the plant quality hypothesis predicts that treatment III should have been preferred during the first two trials (because the newly planted grasses in treatment IV had not yet germinated) and treatment IV thereafter. In fact, treatment II was pre- ferred by deer during the first three trials, treatment III during the next three trials, and treatment IV during the last trial. Hence, the plant quality hypothesis failed in 6/7 trials, a poorer record than one would expect even if deer chose patches at random.

The same kind of reasoning supports both the protein and energy maximization hypotheses. Swards of approx- imately 500-1000 kg/ha dry mass, were predicted to yield the highest rates of protein or energy gain per day (Figs. 1, 2). During the first four trials, treatment II was closest to the optimal biomass range. Both treatments II and III were in the optimal range during the next two tri- als. Treatments III and IV were in the optimal range dur- ing the last trial. These predictions square well with the observed patch preferences: treatment II was preferred during the first three trials, treatment III was preferred during the next three trials and treatment IV was pre- ferred during the last trial. This pattern suggests that the preferred treatment changed over time as some grass patches (e.g. treatment II) grew out of the optimal bio- mass range at the same time as other grass patches (first treatment III and later IV) grew into the optimal range.

O E C O L O G I A 104 (1995) �9 Springer-Verlag 299

8 0 0

6 0 0 LLI

_ 4 0 0

2 0 0

o o

A A

i i �9 �9

2 4 6

FORAGE BIOMASS

Fig. 2 Langvatn and Hanley's (1993) estimates of digestible dry matter intake (o; g min -1) and digestible protein intake (A; g min -1) on each of four vegetation densities (kg/ha x 103) over sev- en foraging trials with red deer

Without access to the original data, this assertion cannot be tested more rigorously, nor can we reject the remote possibility that feeding preferences were determined by concentrations of soluble nitrogen, secondary metabo- lites, or other plant nutrients that were uncorrelated with plant biomass.

The critical difference between our analysis and that of Langvatn and Hanley (1993) is our inclusion of a pro- cessing constraint. Everything else being equal, the availability constraint predicts a positive relationship be- tween DDM intake and grass biomass. This is due to the functional response increasing faster than digestibility declines with increasing grass biomass. While the avail- ability no doubt reflects the short term benefits of patch selection, natural selection should favor behaviors that maximize fitness over longer time scales.

Ultimately, foraging rates in ruminants are limited by the rate of gut clearance, that is, animals could theoreti- cally bite more food than they can process through their digestive tracts. Langvatn and Hanley's (1993) implicit short term model therefore predicts that DDM intake should approach an asymptote at high forage biomass, whereas our long term model predicts a decline in DDM intake with increasing grass biomass (Fig. 2).

Langvatn and Hanley have clearly shown that patch use by red deer is strongly correlated with rates of pro- tein gain. We agree with this result, but also argue that patch use may be as strongly correlated with daily rates of energy gain in red deer, as indicated by our analagous experiments with Cervus elaphus in North America (Wilmshurst et al. 1995). Teasing apart these covarying nutritional currencies may not be a simple matter.

Finally, we note with interest that in Langvatn and Hanley's (1993) experiments and Wilmshurst et al.'s (1995) analogous experiments, deer used patches in pro- portion to fitness gains, rather than concentrating entirely within the best patch. Such matching behavior (some- times termed partial preference behavior) is common even in tightly controlled foraging experiments and is of- ten interpreted as reflecting the necessity of repeated

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sampl ing by animals in order to assess pa tch qual i ty or s imply d i sc r imina t ion errors (Krebs and M c C l e e r y 1984). Indeed, it wou ld be rare in b io logy to see no vari- a t ion around any threshold funct ion, such as op t imal diet se lect ion or op t imal patch select ion (Stephens 1985). It cer ta in ly cannot be regarded as sui table grounds for re- j ec t ion of op t imal i ty models .

Acknowledgements This work was funded by an Ontario Gradu- ate Scholarship to J.EW. and a Natural Science and Engineering Research Council of Canada operating grant to J.M.E We thank Rolf Langvatn, Tom Hanley, and two anonymous reviewers for their critical comments on the manuscript.

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